Temporal fruit microbiome and immunity dynamics in postharvest apple (Malus x domestica)

Abstract

The plant immune response plays a central role in maintaining a well-balanced and healthy microbiome for plant health. However, insights into how the fruit immune response and the fruit microbiome influence fruit health after harvest are limited. We investigated the temporal dynamics of the fruit microbiota and host defense gene expression patterns during postharvest storage of apple fruits at room temperature. Our results demonstrate a temporal dynamic shift in both bacterial and fungal community composition during postharvest storage that coincides with a steep-decline in host defense response gene expression associated with pattern-triggered immunity. We observed the gradual appearance of putative pathogenic/spoilage microbes belonging to genera Alternaria (fungi) and Gluconobacter and Acetobacter (bacteria) at the expense of Sporobolomyces and other genera, which have been suggested to be beneficial for plant hosts. Moreover, artificial induction of pattern-triggered immunity in apple fruit with the flg22 peptide delayed the onset of fruit rot caused by the fungal pathogen Penicillium expansum. Our results suggest that the fruit immune response helps to orchestrate a microbiome and that the collapse of the immunity results in the proliferation of spoilage microbes and fruit rot. These findings hold implications for the development of strategies to increase fruit quality and prolong shelf life in fruits and vegetables.

Acknowledgments

Funding support was provided by Michigan State University AgBioResearch and the Michigan Apple Committee. We thank Cory Outwater for assistance in orchard maintenance and Dr. Tyre Proffer with his assistance in culturing and inoculation of P. expansum. We also want to thank Dr. Kristi MacCready, Dr. Xiaochen Yuan, Dr. Karla Vasco, and Julian Liber for their help in training and troubleshooting problems with data analysis. We thank Jerimiah Johnson, Kirsten Pollok, Ishani Misra, Noah Diaz, Kevin Mclaughlin, and Elise Straub for their help with sample processing. Hannah McMillan is supported by a Postdoctoral Fellowship in Biology from the National Science Foundation (Award Number 2208939). Sheng Yang He is an investigator at Howard Hughes Medical Institute. Roselane Kithan-Lundquist was supported by a fellowship from the US National Institutes of Health Plant Biotechnology for Health and Sustainability Training Program at Michigan State University (Grant nos: NIH T32-GM110523).

Author contributions

GS, SYH, and RK-L conceptualized and designed the experiment. RK-L performed the experiments and analyzed the data. HM contributed to data analysis and interpretation of the results. RK-L wrote the first draft. HM, SYH, and GS provided critical comments and edited the manuscript.

Data availability

Raw data used in this study are available in the NCBI Sequence Read Archive (SRA) under the BioProject IDs: PRJNA1112867 and PRJNA1112895.

Conflict of interest statement

None declared.

Supplementary data

Supplementary data is available at Horticulture Research online.

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